Influence of Food Type on Specific Dynamic Action of the Chinese Skink Eumeces Chinensis
Comparative Biochemistry and Physiology, Part A 140 (2005) 151–155 www.elsevier.com/locate/cbpa
Influence of food type on specific dynamic action of the Chinese skink Eumeces chinensis
Zhi-Chong Pana, Xiang Jib,c,*, Hong-Liang Lub, Xiao-Mei Mab
aDepartment of Biology, School of Life Sciences and Biotechnology, Ningbo University, Ningbo 315211, Zhejiang, People’s Republic of China bDepartment of Environmental Sciences and Natural Resources, School of Life Sciences, Hangzhou Normal College, Hangzhou 310036, Zhejiang, People’s Republic of China cJiangsu Key Laboratory for Bioresource Technology, School of Life Sciences, Nanjing Normal University, Nanjing 210097, Jiangsu, People’s Republic of China
Received 19 September 2004; received in revised form 18 November 2004; accepted 18 November 2004
Abstract
We used the Chinese skink (Eumeces chinensis) as an experimental model to study influence of food type on specific dynamic action (SDA) of feeding. Thirty-three adult males collected from a natural population were divided equally into three (one control and two experimental) groups. We starved all skinks at 30 8C for 3 days and then provided the experimental skinks with a single meal consisting of either mealworms or meat [the flesh of the bullfrog (Rana catesbeiana)]. Food ingested by skinks of the two experimental groups differed in lipid content and lean dry mass but not in total dry mass and energy. Defecation following feeding occurred slightly earlier in skinks ingesting mealworms (mean=41.7 h) than in those ingesting meat (mean=47.7 h), but the difference was not significant. Analyses of variance (ANOVAs) with repeated measures showed that temporal variation in oxygen consumption over 72 h after feeding was evident in the experimental skinks but not in the control ones. Oxygen consumption was higher in the experimental skinks than in the control ones during the time interval between 4.5 and 36 h after feeding. The peak metabolic rate was greater but occurred later in skinks ingesting meat than in those ingesting mealworms. The estimated amounts of oxygen consumed by mealworm-fed, meat-fed and unfed skinks at 30 8C over 72 h after feeding were 356.5, 393.8 and 295.2 mL, respectively. Our results provide a support for the previous prediction that SDA is affected by types of food ingested by animals as skinks ingesting mealworms and meat differed in the time to reach a peak metabolic rate, the level of the peak metabolic rate and the magnitude of the SDA effect. D 2005 Elsevier Inc. All rights reserved.
Keywords: Scincidae; Eumeces chinensis; Food intake; Food type; Oxygen consumption; Specific dynamic action; Energy content; Lipid content
1. Introduction processes of digestion, absorption and assimilation of food (Kleiber, 1961; Bartholomew, 1977; Jobling, 1981, 1983; Animals obtain energy through feeding, and, for those Cruz-Neto et al., 2001; Secor, 2001; Iglesias et al., 2003). that are carrying out a normal pattern of activities, the The postprandial increase in metabolic rate, commonly obtained energy is used not only for basal or standard called for historical reasons specific dynamic action metabolism, thermoregulation, activity and production (tis- (SDA), has been found in all animals so far studied (e.g., sue growth and offspring production) but also for the Jobling, 1981, 1983; Chapelle et al., 1994; Peck, 1996; Guinea and Fernandez, 1997; Rosen and Trites, 1997; Secor and Diamond, 1997a,b; Secor and Phillips, 1997; Cruz-Neto * Corresponding author. Department of Environmental Sciences and et al., 1999; Overgaard et al., 1999; Sievert and Andreadis, Natural Resources, School of Life Sciences, Hangzhou Normal College, Hangzhou 310036, Zhejiang, People’s Republic of China. Tel.: +86 571 1999; Robert and Thompson, 2000; Iglesias et al., 2003; 88989878; fax: +86 571 28865337. Sigsgaard et al., 2003; Pan et al., 2004). SDA is of sufficient E-mail address: [email protected] (X. Ji). magnitude that it must be taken into account in all analyses
1095-6433/$ - see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpb.2004.11.013 152 Z.-C. Pan et al. / Comparative Biochemistry and Physiology, Part A 140 (2005) 151–155 of energy metabolism (Bartholomew, 1977). The general to 38 g and snout-vent length from 100 to 110 mm. The pattern of SDA seems to be similar in most animals and is captured skinks were transported to our laboratory at characterized by a rapid increase in metabolic rate soon after Hangzhou Normal College, where they were divided equally feeding to a peak followed by gradual decreases to the into three [one (unfed) control and two (fed) experimental] prefeeding values (e.g., Jobling, 1981; Chapelle et al., 1994; groups of which each was housed in a 1000Â600Â500 Guinea and Fernandez, 1997; Secor and Phillips, 1997; (lengthÂwidthÂheight) mm3 glass cage. We placed the Robert and Thompson, 2000; Iglesias et al., 2003; Pan et al., cages in a constant temperature room at 30 8C, thereby 2004). However, the time it takes to reach a peak metabolic controlling the mean body temperature of skinks at the rate, the level of the peak metabolic rate and the duration and corresponding level (Ji et al., 1995). Room lights were set to the magnitude of the SDA effect may vary, in various a cycle of 12 light:12 dark. Prior to measuring oxygen degrees, among and within species primarily because the consumption, we starved all skinks for 3 days to ensure a traits involved in the SDA effect are affected by numerous uniform postabsorptive state (Ji et al., 1995; Xu et al., 1999). external and internal factors such as temperature, reproduc- At the end of the 3-day fast, we housed skinks individually tive condition, size, quantity and composition of the meal in 300 mL closed-system respiratory chambers inside which and forage mode (and thus, feeding frequency) (Bennett and the temperature was controlled at 30 8C, and then measured Dawson, 1976; Greene, 1983; Jobling, 1983; Schwarzkopf, oxygen consumption (VO2) for each skink based on the 1991; Secor and Diamond, 1995; Andrade et al., 1997; reduced air space in a calibrated tube during 10 min (Wang McKinon and Alexander, 1999; Robert and Thompson, and Ji, 1997). After measurements, we provided the 2000; Wang et al., 2001, 2002; Whiteley et al., 2001; Iglesias experimental skinks with a single meal consisting of either et al., 2003; Toledo et al., 2003). For example, an increased mealworms (larvae of Tenebrio molitor) or meat [the flesh of food intake prolongs the duration of SDA in Pygoscelis the bullfrog (Rana catesbeiana)]. Our skinks need not to be adeliae (Ade´lie penguin; Janes and Chappell, 1995), trained to eat mealworms and frog meat, although the two increases the magnitude of the SDA effect in Python molurus types of food are novel to them. We allowed the exper- (Albino Burmese python; Secor and Diamond, 1997a,b) and imental skinks to eat voluntarily as much as they wanted for Crotalus durissus (Neotropical rattlesnake; Andrade et al., 1 h, thereby avoiding force-feeding. The first two pieces of 1997) and postpones the time it takes to reach a peak food ingested by the experimental skinks each contained a 3- metabolic rate in Pleuronectes platessa (European plaice; mm blue plastic thread (diameter 0.2 mm), which was used Jobling and Davies, 1980). Animals that ingest food as a mark. The food passage time was defined as the lapsed containing more proteins have a greater magnitude of the time from swallowing to appearance of the first plastic SDA effect (Bartholomew, 1977; Coulson and Hernandez, thread (Ji et al., 1995). We measured oxygen consumption of 1979; Janzen, 1981; Blaxter, 1989; Houlihan, 1991; Chak- both experimental and control skinks over 72 h at time raborty et al., 1992; Secor and Diamond, 1997b). intervals varying from 4.5 to 12 h after the event of feeding As the metabolic response of fasted animals to a single using the same respiratory chambers described above. meal often accurately reflects energetic costs of digestion, We extracted nonpolar lipids from dried samples of food absorption and assimilation of food, measuring temporal in a Soxhlet apparatus for a minimum of 5.5 h using variation in oxygen consumption after feeding is a absolute ether as solvent. The amount of lipids in each commonly used method to test for the SDA effect in sample was determined by subtracting the lipid-free dry animals (Jobling, 1981; Janes and Chappell, 1995; Sievert mass from the total sample dry mass. We determined energy and Bailey, 2000). In the present study, we investigate the density of dried samples of food using a WGR-1 adiabatic differential postprandial metabolic response (SDA) of bomb calorimeter (Changsha Bente Instruments, China). Chinese skinks (Eumeces chinensis) to different food. Our Titrations were performed on the residue after calorimetry to experimental model is a medium-sized (up to 134 mm SVL) correct for nitrogenous wastes. Further corrections were ground-dwelling oviparous scincid lizard, which is one of performed for fuse wire burning. most conspicuous lizard species in the southern provinces All data were tested for normality (Kolmogorov–Smir- (including Taiwan and Hainan) of China (Zhao and Adler, nov test) and homogeneity of variances (Bartlett test), and 1993; Lin and Ji, 2000; Ji et al., 2002). Our aims are (1) to Loge transformations were performed when necessary to show the general pattern of SDA in E. chinensis, (2) to satisfy the assumptions for parametric tests. We used one- examine influence of food type on SDA and (3) to compare way analyses of variance (ANOVA) and repeated-measures our data with those collected in other parallel studies. ANOVA to analyze the corresponding data when the assumptions of parametric analyses were met. Nonparamet- ric analyses (Mann–Whitney U-test) were used when these 2. Materials and methods assumptions were violated. The magnitude of the SDA effect was estimated to be equal to the area under the curve Thirty-three adult male E. chinensis were collected in from a fit of least squares on the original data of the early August 2003 from a population in the vicinity of Lishui experimental group (i.e., total oxygen consumed) minus the (Zhejiang, eastern China), with body mass varying from 21 area under the curve of the control group (i.e., oxygen Z.-C. Pan et al. / Comparative Biochemistry and Physiology, Part A 140 (2005) 151–155 153 consumed due to resting metabolism). Descriptive statistics are presented as meanF1 standard error, and the signifi- cance level is set at a=0.05.
3. Results
Skinks of the three groups did not differ in size (snout- vent length) and mass (one-way ANOVA, both PN0.921). Food ingested by skinks of the two experimental groups differed considerably in wet mass, lipid content and lean dry mass but not in total dry mass and energy content (Table 1). Food passage time (an indicative of defecation following feeding) was apparently shorter in skinks ingesting meal- worms (41.7F4.1 h, N=11) than in those ingesting meat (47.7F3.2 h, N=11), but the difference was not significant ( F1, 20=1.32, P=0.264). The peak metabolic rate was greater Fig. 1. Oxygen consumption (measured at 30 8C) of adult male E. chinensis F F b (8.3 0.4 vs. 6.3 0.2 mL/h O2; F1, 20=16.81, P 0.001) but after a single meal. Error bars are F1 standard error. The differences in occurred about 5 h later (14.3F0.8 vs. 19.4F1.2 h; F1, oxygen consumption between the two experimental groups are examined at 20=11.78, Pb0.003) in skinks ingesting meat than in those each time interval using a one-way ANOVA, and the two means differing ingesting mealworms (Fig. 1). significantly are marked by an asterisk (a=0.05). The curves in the figure are generated from a fit of least squares on the original data, and the Neither body size nor body mass was correlated with horizontal line represents the mean oxygen consumption of the control oxygen consumption measured at each time interval in both skinks. Arrows show the means of food passage time. control and experiments skinks (all PN0.05), so the two potential covariates were excluded from considerations. ingesting meat; the total amount of oxygen consumed by the ANOVAs with repeated measures showed that temporal control skinks was 295.2 mL (4.1 mL/hÂ72 h) (Fig. 1). variation in oxygen consumption over 72 h after feeding Thus, the estimated magnitude of the SDA effect was 61.3 was evident in the experimental skinks (mealworm: F10, mL O2 in skinks ingesting mealworms and 98.6 mL O2 in 100=12.44, Pb0.0001; meat: F10, 100=21.76, Pb0.0001), but those ingesting meat. Assuming that 1 mL O2 releases 20.08 not in the control ones ( F10, 100=0.40, P=0.942). Oxygen J(Schmidt-Nielsen, 1990), energy expended due to SDA consumption of the control skinks averaged 4.1 mL/h O2 was about 1.2 kJ (8.5% of the gross energy content of the (Fig. 1). During the time interval between 4.5 and 36 h after meal) in skinks ingesting mealworms and about 2.0 kJ feeding, oxygen consumption was significantly higher in the (16.9% of the gross energy content of the meal) in skinks experimental skinks than in the control ones (one-way ingesting meat. ANOVA, all Pb0.05), and, within the interval, skinks ingesting meat consumed significantly more oxygen than did those ingesting mealworms measured at 18, 24 and 30 h 4. Discussion after feeding (one-way ANOVA, all Pb0.03) (Fig. 1). The total amount of oxygen consumed, estimated by the The pattern of SDA in E. chinensis is similar to that area under the curve of the experimental group, was 356.5 reported for numerous other animals so far studied using mL in skinks ingesting mealworms and 393.8 mL in those the method of a single meal in that metabolic rate increases
Table 1 Major components of food on which skinks fed in a single meal Mealworm (larvae of Meat (flesh of Rana Significant levels of Tenebrio molitor (N=11) catesbeiana)(N=11) Mann–Whitney U-test Food wet mass (g) 1.49F0.10 2.61F0.04 Pb0.0001 0.99À1.92 2.32À2.79 Food dry mass (mg) 542.9F37.2 545.3F8.3 P=0.922 359.8À700.8 485.9À584.1 Lipid contents (mg) 156.4F10.7 5.3F0.1 Pb0.0001 103.6À201.8 4.8À5.7 Food lean dry mass (mg) 386.6F26.5 540.0F8.3 Pb0.001 256.2À499.0 481.1À578.4 Food energy contents (kJ) 14.1F1.0 11.8F0.2 P=0.082 9.4À18.2 10.5À12.6 Data are expressed as meanF1 standard error and range. 154 Z.-C. Pan et al. / Comparative Biochemistry and Physiology, Part A 140 (2005) 151–155 soon after feeding to a peak and then decreases to the (Robert and Thompson, 2000), 50 h in E. quoyii (Iglesias et prefeeding values (Fig. 1). However, the time to reach a al., 2003), 15 h in S. indicus (Lu et al., 2004) and 28 h in peak metabolic rate, the level of the peak metabolic rate hatchlings of T. s. elegans (Pan et al., 2004). The above and the magnitude of the SDA effect differed between comparisons show that the time it takes to reach a peak skinks ingesting mealworms and meat (Fig. 1). The metabolic rate, the level of the peak metabolic rate and the duration of the SDA effect did not differ between the two duration of the SDA effect differ among reptiles even fed experimental groups because the time intervals (4.5–36 h) with the same food. Actually, inter- and intraspecific when the experimental skinks consumed significantly more differences in the SDA effect are very obvious when oxygen than did control ones did not differ between the two comparing data collected in a variety of animals from groups. Food intake (both dry mass and energy content) did vertebrates to invertebrates that ingest food differing in both not differ significantly between the two experimental quality (and thus, composition) and quantity (e.g., Jobling groups (Table 1), so the confounding effect resulting from and Davies, 1980; Janes and Chappell, 1995; Peck, 1996; variation in food intake can be lessened to some extent. As Andrade et al., 1997; Rosen and Trites, 1997; Secor and food ingested by skinks of the two experimental groups Diamond, 1997a,b; Ferry-Graham and Gibb, 2001; White- differed considerably in wet mass, lipid content and lean ley et al., 2001; Sigsgaard et al., 2003). For example, dry mass, our results therefore add evidence that food type feeding can be followed by a 10–45-fold increase in oxygen (and thus, source of nutrients) can influence SDA of consumption in some species (such as snakes) that occa- animals (e.g., Secor and Phillips, 1997; Somanath et al., sionally ingest very large meals (Secor and Diamond, 1995; 2000; Pan et al., 2004). Andrade et al., 1997; Overgaard et al., 1999; Bedford and Metabolic rate rose by up to about 1.5 times prefeeding Christian, 2001; Toledo et al., 2003), but the elevated values within 14.3 h at 30 8C in skinks ingesting meal- metabolic rate after feeding is much less pronounced in worms and to about 2.0 times prefeeding values within 19.4 animals that ingest small meals or feed more frequently h in skinks eating meat (Fig. 1). This difference results (Overgaard et al., 1999; Bedford and Christian, 2001; primarily from the differential energetic costs associated Iglesias et al., 2003). However, as food intake was with digestion, absorption and assimilation of different food. expressed in terms of mass rather than energy in most As SDA is about 4–30% for carbohydrates, 4–15% for previous studies, whether variation in the SDA effect fats and 30–70% for proteins when it is expressed in terms reflects the accumulative or the combined effects of of the energy content of the food ingested (Bartholomew, individual nutrient components in the ingested food still 1977; Blaxter, 1989), the magnitude of the SDA effect remains an unanswered question. should be therefore more pronounced in animals ingesting more proteins. Given that skinks of the two experimental groups did not differ significantly in the duration of the Acknowledgements SDA effect and the total ingested energy, the greater magnitude of the SDA effect in skinks ingesting meat is The Zhejiang Provincial Bureau of Forestry provided us therefore primarily due to the lower lipid content (and thus, an official permit to collect Chinese skinks from the field. more proteins) in this type of food (Table 1). We thank the following people for assistance both in the When comparing our data with those collected in other field and in the laboratory: Hui-Li Chen, Jian-Fang Gao, parallel studies in which food ingested by reptiles main- Long-Hui Lin, Zhi-Hua Lin, Lai-Gao Luo, Xiang Shen and tained at 30 8C in a single meal consisting of mealworms, Er Zhang for their continuous help during the research. we find that the influence of individual variables involved in Financial supports for this research were provided by the the SDA effect, in various degrees, differs among species. local government of Zhejiang Province for the Specially The time it took to reach a peak metabolic rate was about 4 Supported Discipline of Zoology to XJ. hinEulamprus tympanum (southern water skink; Robert and Thompson, 2000), 15 h in E. quoyii (eastern water skink; Iglesias et al., 2003), 13 h in Sphenomorphus indicus References (brow forest skink; Lu et al., 2004) and 10 h in hatchling Trachemys scripta elegans (red-eared slider turtle; Pan et Andrade, D.V., Cruz-Neto, A.P., Abe, A.S., 1997. 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